Anatomy and Histochemistry of Spread-Wing Posture in Birds. I. Wing Drying Posture in the Double-Crested Cormorant, Phalacrocorax auritus

Spread-wing postures of birds often have been studied with respect to the function of behavior, but ignored with regard to the mechanism by which the birds accomplish posture. The double-crested cormorant, Phalacrocorax auritus, was used as a model for this study of spread-wing posture. Those muscles capable of positioning and maintaining the wing in extension and protraction were assayed histochemically for the presence of slow (postural) muscle fibers.Within the forelimb of Phalacrocorax,Mm. coracobrachialis cranialis, pectoralis thoracicus (cranial portion), deltoideus minor, triceps scapularis, and extensor metacarpi radialis pars dorsalis and ventralis were found to contain populations of slow-twitch or slow-tonic muscle fibers. These slow fibers in the above muscles are considered to function during spreadwing posture in this species. J Morphol 233:67–76, 1997. r 1997 Wiley-Liss, Inc. Birds and mammals possess specializations of the musculoskeletal system to reduce the cost of a variety of behaviors. For example, the horse passive stay apparatus (Dyce et al., ’87) and albatross shoulder lock (Pennycuick, ’82) reduce the overall need for muscle contraction during long-term standing and soaring, respectively. Slow-contracting muscle fibers are specialized for sustained contraction and high fatigue resistance (Goldspink, ’77), and can be found in muscles associated with posture. Slow fibers are more efficient at postural (isometric) contractions due to the longer interactions between actin and myosin and the resulting decreased cost ofATP.Within birds, slow fibers have been described as making up a deep layer of the pectoralis muscle of turkey vultures (Cathartes aura; Rosser and George, ’86a) and white pelicans (Pelecas erythrorhynchos; Rosser et al., ’94) as a specialization formaintainingwing posture during soaring flight. These fibers have been hypothesized to be present in the pectoralis of all gliding and soaring species (Pennycuick, ’72, ’82; Meyers, ’93). In addition, a suite of slow shoulder muscles function to keep the avian wing in a folded position (Meyers, ’92). Both spread-wing and foldedwing behaviors present relatively long-term mechanical events that are made ‘‘lessexpensive’’ by the presence of slow-muscle fiber types. Whereas slow-muscle specializations have been described for mammal limbs (which must bear weight constantly when the animal is standing; e.g., see Armstrong, ’80; Hermanson et al., ’91; Suzuki, ’91; Petrie et al., ’93), such modifications in the avian forelimb are less often encountered. In part this is due to the fact that in contrast to the mammalian forelimb, the avian wing does not normally bear weight when at rest. The spread-wing posture of cormorants and other birds is one behavior that could be facilitated by the reduced energetic cost of slowmuscle fibers.Although this behavior is believed to function in drying the wings of cormorants (Hennemann, ’84, ’88; see Simmons, ’86, for review), the actual means by which these birds hold the wings spread to perform this behavior has not been addressed. The double-crested cormorant, Phalacrocorax auritus, was selected for this study because it represents a readily obtainable species that illustrates the spread-wing posture (Bent, ’22). Previous studies on cormorant forelimb morphology (Owre, ’67; Livezey, ’92) have not commented on pos*Correspondence to: Ron A. Meyers, Department of Zoology, Weber State University, Ogden, UT 84408-2505. JOURNAL OF MORPHOLOGY 233:67–76 (1997) r 1997 WILEY-LISS, INC. sible muscle function during spread-wing posture. The goal of this study is to examine those forelimb muscles of Phalacrocorax auritus capable of positioning the spread wing, and to assess which muscles contain slowcontracting (postural) fibers. MATERIALS AND METHODS Two individuals of Phalacrocorax auritus (obtained from the Louisiana State University Museum of Zoology and North Carolina State Museum of Natural History) were dissected to identify whichmuscles were biomechanically suited to function during spreadwing posture. Dissections were illustrated with a Holbein camera lucida. Nomenclature follows that of Meyers (’93) for the muscles and Nomina Anatomica Avium (Baumel and Witmer, ’93) for the skeleton. Fresh muscle samples from three birds were obtained via shooting in the Cape Fear River, North Carolina, under possession of valid state and federal permits. Muscle samples were immediately removed mid-belly, quickfrozen by immersion into isopentane cooled to about 2150°C in liquid nitrogen, and stored at 270°C. Transverse serial sections (10–12 μm thickness) were cut on a freezing cryostat at 220°C and mounted on glass slides for staining. Histochemical staining for myosin ATPase followed the protocol of Staron et al. (’83), which permits the differentiation of slow-twitch, fast-twitch, and slow-tonic fibers (Hikida, ’87) (see Figs. 1, 2). Hikida (’87) has shown that pectoralis, biventer cervicis, and cranial latissimus dorsi muscles from rock doves (pigeons; Columba livia) consist of fast-twitch, mixed fasttwitch/slow-twitch, and slow-tonic muscle fibers, respectively. In the present study, these Fig. 1. Phalacrocorax auritus. Serial sections of ATPase histochemistry of M. extensor metacarpi radialis. a: Alkaline preincubation (pH 10.4). b: Acidic preincubation (pH 4.2). c: Anti-fast antibody (MY32). d: Anti-slow antibody (S58). 1, slow-twitch fiber; 2, fast-twitch fiber. The positive (dark) reaction in acidic preincubation corresponds with positive anti-slow antibody reaction and that positive reaction in alkaline preincubation corresponds with anti-fast antibody reaction product. Note that in d an adjacent area of fibers is shown. Scale 5 100 μm. 68 R.A. MEYERS